Modulation of the cold-activated channel TRPM8 by lysophospholipids and polyunsaturated fatty acids

Journal of Neuroscience

Volumn 27, Issue 12, 2007, Pages 3347-3355

  Andersson, David A ^a,b   Nash, Mark ^b,c   Bevan, Stuart ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Novartis Inst for Medical Sciences   (United Kingdom)

^c Novartis Institute for Biomedical Sciences   (United Kingdom)

Author keywords

Arachidonic acid; Icilin; Lysophospholipid; Menthol; Phospholipase A2; TRPM8

Indexed keywords

ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; INOSITOL DERIVATIVE; LYSOPHOSPHATIDYLCHOLINE; LYSOPHOSPHATIDYLSERINE; LYSOPHOSPHOLIPID; MENTHOL; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; POLYUNSATURATED FATTY ACID; PROTEIN TRPM8; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; DRUG EFFECT; ENZYME INHIBITION; HEAT SENSITIVITY; NONHUMAN; OVARY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD NERVE CELL; SPINAL GANGLION; TEMPERATURE SENSITIVITY;

ANIMALS; CHO CELLS; COLD; CRICETINAE; CRICETULUS; DOSE-RESPONSE RELATIONSHIP, DRUG; FATTY ACIDS, UNSATURATED; FEMALE; LYSOPHOSPHOLIPIDS; MALE; MICE; RATS; RATS, WISTAR; TRPM CATION CHANNELS;

EID: 33947515995     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4846-06.2007     Document Type: Article

References (48)

1. Abeele FV, Zholos A, Bidaux G, Shuba Y, Thebault S, Beck B, Flourakis M, Panchin Y, Skryma R, Prevarskaya N (2006) Ca(2+)-independent phospholipase A(2)-dependent gating of TRPM8 by lysophospholipids. J Biol Chem 281:40174-40182.
2. Andersson DA, Chase HW, Bevan S (2004) TRPM8 activation by menthol, icilin, and cold is differentially modulated by intracellular pH. J Neurosci 24:5364-5369.
3. Babes A, Zorzon D, Reid G (2004) Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur J Neurosci 20:2276-2282.
4. Balsinde J, Balboa MA (2005) Cellular regulation and proposed biological functions of group VIA calcium-independent phospholipase A2 in activated cells. Cell Signal 17:1052-1062.
5. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-857.
6. Bevan S, Winter J (1995) Nerve growth factor (NGF) differentially regulates the chemosensitivity of adult rat cultured sensory neurons. J Neurosci 15:4918-4926.
7. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
8. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436-441.
9. Chuang HH, Neuhausser WM, Julius D (2004) The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43:859-869.
10. Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517-524.
11. Flemming PK, Dedman AM, Xu SZ, Li J, Zeng F, Naylor J, Benham CD, Bateson AN, Muraki K, Beech DJ (2006) Sensing of lysophospholipids by TRPC5 calcium channel. J Biol Chem 281:4977-4982.
12. Fuentes L, Perez R, Nieto ML, Balsinde J, Balboa MA (2003) Bromoenol lactone promotes cell death by a mechanism involving phosphatidate phosphohydrolase-1 rather than calcium-independent phospholipase A2. J Biol Chem 278:44683-44690.
13. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22:6408-6414.
14. Hara Y, Wakamori M, Ishii M, Maeno E, Nishida M, Yoshida T, Yamada H, Shimizu S, Mori E, Kudoh J, Shimizu N, Kurose H, Okada Y, Imoto K, Mori Y (2002) LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell 9:163-173.
15. Hardie RC (2003) Regulation of TRP channels via lipid second messengers. Annu Rev Physiol 65:735-759.
16. Hu HZ, Xiao R, Wang C, Gao N, Colton CK, Wood JD, Zhu MX (2006) Potentiation of TRPV3 channel function by unsaturated fatty acids. J Cell Physiol 208:201-212.
17. Huang CL, Feng S, Hilgemann DW (1998) Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 391:803-806.
18. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, Cho S, Min KH, Suh YG, Kim D, Oh U (2000) Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97:6155-6160.
19. Jordt SE, McKemy DD, Julius D (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13:487-492.
20. Kita Y, Ohto T, Uozumi N, Shimizu T (2006) Biochemical properties and pathophysiological roles of cytosolic phospholipase A(2)s. Biochim Biophys Acta 1761:1317-1322.
21. Lanni C, Becker EL (1985) Inhibition of neutrophil phospholipase A2 by p-bromophenylacyl bromide, nordihydroguaiaretic acid, 5,8,11,14-eicosatetraynoic acid and quercetin. Int Arch Allergy Appl Immunol 76:214-217.
22. Lesage F, Terrenoire C, Romey G, Lazdunski M (2000) Human TREK2, a 2P domain mechano-sensitive K+ channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq protein-coupled receptors. J Biol Chem 275:28398-28405.
23. Liu B, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:1674-1681.
24. Liu D, Liman ER (2003) Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci USA 100:15160-15165.
25. Maingret F, Patel AJ, Lesage F, Lazdunski M, Honore E (2000) Lysophospholipids open the two-pore domain mechano-gated K(+) channels TREK-1 and TRAAK. J Biol Chem 275:10128-10133.
26. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58.
27. Mukerji G, Yiangou Y, Corcoran SL, Selmer IS, Smith GD, Benham CD, Bountra C, Agarwal SK, Anand P (2006) Cool and menthol receptor TRPM8 in human urinary bladder disorders and clinical correlations. BMC Urol 6:6.
28. Patapoutian A, Peier AM, Story GM, Viswanath V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4:529-539.
29. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002a) ATRP channel that senses cold stimuli and menthol. Cell 108:705-715.
30. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, Patapoutian A (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046-2049.
31. Reid G, Flonta ML (2001) Physiology. Cold current in thermoreceptive neurons. Nature 413:480.
32. Reid G, Flonta ML (2002) Ion channels activated by cold and menthol in cultured rat dorsal root ganglion neurones. Neurosci Lett 324:164-168.
33. Rohacs T, Lopes CM, Michailidis I, Logothetis DE (2005) PI(4,5)P(2) regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8:626-634.
34. Runnels LW, Yue L, Clapham DE (2002) The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat Cell Biol 4:329-336.
35. Seno K, Okuno T, Nishi K, Murakami Y, Yamada K, Nakamoto S, Ono T (2000) Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J Med Chem 43:1041-1044.
36. Singaravelu K, Lohr C, Deitmer JW (2006) Regulation of store-operated calcium entry by calcium-independent phospholipase A2 in rat cerebellar astrocytes. J Neurosci 26:9579-9592.
37. Smani T, Zakharov SI, Csutora P, Leno E, Trepakova ES, Bolotina VM (2004) A novel mechanism for the store-operated calcium influx pathway. Nat Cell Biol 6:113-120.
38. Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P, Facer P, Wright JE, Jerman JC, Walhin JP, Ooi L, Egerton J, Charles KJ, Smart D, Randall AD, Anand P, Davis JB (2002) TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418:186-190.
39. Stein RJ, Santos S, Nagatomi J, Hayashi Y, Minnery BS, Xavier M, Patel AS, Nelson JB, Futrell WJ, Yoshimura N, Chancellor MB, De Miguel F (2004) Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract. J Urol 172:1175-1178.
40. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like Channel Expressed in Nociceptive Neurons, Is Activated by Cold Temperatures. Cell 112:819-829.
41. Togashi K, Hara Y, Tominaga T, Higashi T, Konishi Y, Mori Y, Tominaga M (2006) TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25:1804-1815.
42. Tsavaler L, Shapero MH, Morkowski S, Laus R (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61:3760-3769.
43. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748-754.
44. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424:434-438.
45. Wilson-Ashworth HA, Judd AM, Law RM, Freestone BD, Taylor S, Mizukawa MK, Cromar KR, Sudweeks S, Bell JD (2004) Formation of transient non-protein calcium pores by lysophospholipids in S49 Lymphoma cells. J Membr Biol 200:25-33.
46. Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, Ge P, Lilly J, Silos-Santiago I, Xie Y, DiStefano PS, Curtis R, Clapham DE (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418:181-186.
47. Zhang L, Jones S, Brody K, Costa M, Brookes SJ (2004) Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. Am J Physiol Gastrointest Liver Physiol 286:G983-G991.
48. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di M, V, Julius D, Hogestatt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452-457.